Rickettsial Infections among Cats and Cat Fleas in Riverside County, California

Kristin E. Mullins Naval Medical Research Center, Silver Spring, Maryland;
University of Maryland School of Medicine, Baltimore, Maryland;

Search for other papers by Kristin E. Mullins in
Current site
Google Scholar
PubMed
Close
,
Alice N. Maina Naval Medical Research Center, Silver Spring, Maryland;

Search for other papers by Alice N. Maina in
Current site
Google Scholar
PubMed
Close
,
Laura Krueger Orange County Mosquito and Vector Control District, Garden Grove, California;

Search for other papers by Laura Krueger in
Current site
Google Scholar
PubMed
Close
,
Ju Jiang Naval Medical Research Center, Silver Spring, Maryland;

Search for other papers by Ju Jiang in
Current site
Google Scholar
PubMed
Close
,
Robert Cummings Orange County Mosquito and Vector Control District, Garden Grove, California;

Search for other papers by Robert Cummings in
Current site
Google Scholar
PubMed
Close
,
Allan Drusys Riverside County Department of Animal Services, Riverside, California;

Search for other papers by Allan Drusys in
Current site
Google Scholar
PubMed
Close
,
Greg Williams Northwest Mosquito and Vector Control District, Corona, California;

Search for other papers by Greg Williams in
Current site
Google Scholar
PubMed
Close
,
Major Dhillon Northwest Mosquito and Vector Control District, Corona, California;

Search for other papers by Major Dhillon in
Current site
Google Scholar
PubMed
Close
, and
Allen L. Richards Naval Medical Research Center, Silver Spring, Maryland;
Uniformed Services University of the Health Sciences, Bethesda, Maryland

Search for other papers by Allen L. Richards in
Current site
Google Scholar
PubMed
Close
Restricted access

Presently, few studies have investigated the role of domestic cats (Felis catus) in the recrudescence of flea-borne rickettsioses in California and the southern United States. In this study, we aimed to investigate the presence of Rickettsia typhi or Rickettisa felis in domestic cats (F. catus) and the fleas (primarily Ctenocephalides felis, the cat flea) associated with these cats in Riverside County, California. Thirty cats and 64 pools of fleas collected from these cats were investigated for rickettsial infections. Three cats and 17 flea pools (from 10 cats) tested positive for rickettsial infections. polymerase chain reaction and DNA sequencing indicated that one of the cats was positive for R. felis infections, whereas two were positive for Candidatus Rickettsia senegalensis infection. In addition, 12 of the flea pools were positive for R. felis, whereas five were positive for Ca. R. senegalensis. By contrast, no cats or their associated fleas tested positive for R. typhi. Finally, eight sera from these cats contained spotted fever group Rickettsia (SFGR) antibodies. The detection of R. felis and SFGR antibodies and the lack of R. typhi and TGR antibodies support R. felis as the main rickettsial species infecting cat fleas. The detection of Ca. R. senegalensis in both fleas and cats also provides additional evidence that cats and their associated fleas are infected with other R. felis–like organisms highlighting the potential risk for human infections with R. felis or R. felis–like organisms.

Author Notes

Address correspondence to Kristin E. Mullins, School of Medicine, University of Maryland, 685 West Baltimore Street, Baltimore, MD 21201. E-mail: kmullins@som.umaryland.edu

Financial support: This work was supported by U.S. Department of Defense Global Emerging Infections Surveillance and Response System (GEIS), work unit number 847705.82000.25GB.A0074.

Copyright statement: I am an employee of the U.S. Government (A. L. R.) and this work was prepared as part of my official duties. Title 17 U.S.C. §105 provides that “Copyright protection under this title is not available for any work of the United States Government.” Title 17 U.S.C. §101 defines a U.S. Government work as a work prepared by a military service member or employee of the U.S. Government as part of that person’s official duties.

Authors’ addresses: Kristin E. Mullins, School of Medicine, University of Maryland, Baltimore, MD, E-mail: kmullins@som.umaryland.edu. Alice N. Maina, Ju Jiang, and Allen L. Richards, Naval Medical Research Center, Silver Spring, MD, E-mails: alice.n.maina.ctr@mail.mil, ju.jiang2.ctr@mail.mil, and allen.l.richards.civ@mail.mil. Laura Krueger and Robert Cummings, Orange County Mosquito and Vector Control District, Garden Grove, CA, E-mails: lkrueger@ocvcd.org and rcummings@ocvcd.org. Allan Drusys, Riverside County Department of Animal Services, Riverside, CA, E-mail: adrusys@rivco.org. Greg Williams and Major Dhillon, Northwest Mosquito and Vector Control District, Corona, CA, E-mails: gwilliams@northwestmvcd.org and mdhillon@northwestmvcd.org.

  • 1.

    Meleney HE, French RS, 1945. Endemic typhus fever in southern California. Cal West Med 62: 116119.

  • 2.

    Meleney HE, 1941. Recent extension of endemic typhus fever in the southern United States. Am J Public Health Nations Health 31: 219227.

  • 3.

    Brill IC, 1917. Typhus exanthematicus in San Francisco. Cal State. J Med 15: 2930.

  • 4.

    Kligler IJ, Aschner M, Levine S, 1936. Comparative studies of the louse-borne (epidemic) and flea-borne (murine) typhus viruses. Br J Exp Pathol 17: 5360.

  • 5.

    Hill EL, Morlan HB, Utterback BC, Schubert JH, 1951. Evaluation of county-wide DDT dusting operations in murine typhus control (1946 through 1949). Am J Public Health 41: 396401.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Adams JR, Schmidtmann ET, Azad AF, 1990. Infection of colonized cat fleas, Ctenocephalides felis (Bouche), with a Rickettsia-like microorganism. Am J Trop Med Hyg 43: 400409.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Azad AF, 1990. Epidemiology of murine typhus. Annu Rev Entomol 35: 553569.

  • 8.

    Civen R, Ngo V, 2008. Murine typhus: an unrecognized suburban vectorborne disease. Clin Infect Dis 46: 913918.

  • 9.

    Cowan G, 2000. Rickettsial diseases: the typhus group of fevers—a review. Postgrad Med J 76: 269272.

  • 10.

    Schriefer ME, Sacci JB Jr., Taylor JP, Higgins JA, Azad AF, 1994. Murine typhus: updated roles of multiple urban components and a second typhuslike Rickettsia. J Med Entomol 31: 681685.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Abramowicz KF, Rood MP, Krueger L, Eremeeva ME, 2011. Urban focus of Rickettsia typhi and Rickettsia felis in Los Angeles, California. Vector Borne Zoonotic Dis 11: 979984.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Azad AF, Radulovic S, Higgins JA, Noden BH, Troyer JM, 1997. Flea-borne rickettsioses: ecologic considerations. Emerg Infect Dis 3: 319327.

  • 13.

    Sorvillo FJ, Gondo B, Emmons R, Ryan P, Waterman SH, Tilzer A, Andersen EM, Murray RA, Barr R, 1993. A suburban focus of endemic typhus in Los Angeles County: association with seropositive domestic cats and opossums. Am J Trop Med Hyg 48: 269273.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Eremeeva ME et al. 2012. Two pathogens and one disease: detection and identification of flea-borne rickettsiae in areas endemic for murine typhus in California. J Med Entomol 49: 14851494.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Karpathy SE et al. 2009. Detection of Rickettsia felis and Rickettsia typhi in an area of California endemic for murine typhus. Clin Microbiol Infect 15 (Suppl 2): 218219.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Rust MK, Dryden MW, 1997. The biology, ecology, and management of the cat flea. Annu Rev Entomol 42: 451473.

  • 17.

    Title 17, California Code of Regulations and Reportable Disease Conditions, Rickettsial Diseases. Available at: https://www.cdph.ca.gov/Programs/CID/DCDC/CDPH%20Document%20Library/ReportableDiseases.pdf. Accessed November 24, 2017.

    • PubMed
    • Export Citation
  • 18.

    California Department of Public Health, 2018. Human Flea-Borne Typhus Cases in California 2001–2017. Sacramento, California. Available at: https://www.cdph.ca.gov/Programs/CID/DCDC/CDPH%20Document%20Library/Flea-borneTyphusCaseCounts.pdf. Accessed November 24, 2017.

    • PubMed
    • Export Citation
  • 19.

    Abramowicz KF, Wekesa JW, Nwadike CN, Zambrano ML, Karpathy SE, Cecil D, Burns J, Hu R, Eremeeva ME, 2012. Rickettsia felis in cat fleas, Ctenocephalides felis parasitizing opossums, San Bernardino County, California. Med Vet Entomol 26: 458462.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Maina AN et al. 2016. Rickettsial infections among Ctenocephalides felis and host animals during a flea-borne rickettsioses outbreak in Orange County, California. PLoS One 11: e0160604.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    Schriefer ME, Sacci JB Jr., Dumler JS, Bullen MG, Azad AF, 1994. Identification of a novel rickettsial infection in a patient diagnosed with murine typhus. J Clin Microbiol 32: 949954.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Parola P, 2011. Rickettsia felis: from a rare disease in the USA to a common cause of fever in sub-Saharan Africa. Clin Microbiol Infect 17: 9961000.

  • 23.

    Pérez-Osorio CE, Zavala-Velázquez JE, León JJA, Zavala-Castro JE, 2008. Rickettsia felis as emergent global threat for humans. Emerg Infect Dis 14: 10191023.

  • 24.

    Zavala-Castro J, Zavala-Velázquez J, Walker D, Pérez-Osorio J, Peniche-Lara G, 2009. Severe human infection with Rickettsia felis associated with hepatitis in Yucatan, Mexico. Int J Med Microbiol 299: 529533.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Richards AL, Jiang J, Omulo S, Dare R, Abdirahman K, Ali A, Sharif SK, Feikin DR, Breiman RF, Njenga MK, 2010. Human infection with Rickettsia felis, Kenya. Emerg Infect Dis 16: 10811086.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Billeter SA, Metzger ME, 2017. Limited evidence for Rickettsia felis as a cause of zoonotic flea-borne rickettsiosis in southern California. J Med Entomol 54: 47.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Wiggers RJ, Martin MC, Bouyer D, 2005. Rickettsia felis infection rates in an east Texas population. Tex Med 101: 5658.

  • 28.

    Pieracci EG, Evert N, Drexler NA, Mayes B, Vilcins I, Huang P, Campbell J, Behravesh CB, Paddock CD, 2017. Fatal flea-borne typhus in Texas: a retrospective case series, 1985–2015. Am J Trop Med Hyg 96: 10881093.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Christou C, Psaroulaki A, Antoniou M, Toumazos P, Ioannou I, Mazeris A, Chochlakis D, Tselentis Y, 2010. Rickettsia typhi and Rickettsia felis in Xenopsylla cheopis and Leptopsylla segnis parasitizing rats in Cyprus. Am J Trop Med Hyg 83: 13011304.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Eremeeva ME, Warashina WR, Sturgeon MM, Buchholz AE, Olmsted GK, Park SY, Effler PV, Karpathy SE, 2008. Rickettsia typhi and R. felis in rat fleas (Xenopsylla cheopis), Oahu, Hawaii. Emerg Infect Dis 14: 16131615.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Matthewman L, Kelly P, Hayter D, Downie S, Wray K, Bryson N, Rycroft A, Raoult D, 1997. Domestic cats as indicators of the presence of spotted fever and typhus group rickettsiae. Eur J Epidemiol 13: 109111.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Wedincamp J Jr., Foil LD, 2000. Infection and seroconversion of cats exposed to cat fleas (Ctenocephalides felis Bouche) infected with Rickettsia felis. J Vector Ecol 25: 123126.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    American Veterinary Medical Association, 2013. AVMA Guidelines for the Euthanasia of Animals: 2013 Edition. Available at: https://www.avma.org/KB/Policies/Documents/euthanasia.pdf. Accessed November 24, 2017.

    • PubMed
    • Export Citation
  • 34.

    Jiang J, Stromdahl EY, Richards AL, 2012. Detection of Rickettsia parkeri and Candidatus Rickettsia andeanae in Amblyomma maculatum Gulf Coast ticks collected from humans in the United States. Vector Borne Zoonotic Dis 12: 175182.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35.

    Henry KM, Jiang J, Rozmajzl PJ, Azad AF, Macaluso KR, Richards AL, 2007. Development of quantitative real-time PCR assays to detect Rickettsia typhi and Rickettsia felis, the causative agents of murine typhus and flea-borne spotted fever. Mol Cell Probes 21: 1723.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Leulmi H, Socolovschi C, Laudisoit A, Houemenou G, Davoust B, Bitam I, Raoult D, Parola P, 2014. Detection of Rickettsia felis, Rickettsia typhi, Bartonella species and Yersinia pestis in fleas (Siphonaptera) from Africa. PLoS Negl Trop Dis 8: e3152.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    Jiang J et al. 2013. Molecular detection of Rickettsia felis and Candidatus rickettsia asemboensis in fleas from human habitats, Asembo, Kenya. Vector Borne Zoonotic Dis 13: 550558.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38.

    Tamura K, Stecher G, Peterson D, Filipski A, Kumar S, 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30: 27252729.

  • 39.

    Graf PC, Chretien JP, Ung L, Gaydos JC, Richards AL, 2008. Prevalence of seropositivity to spotted fever group rickettsiae and Anaplasma phagocytophilum in a large, demographically diverse US sample. Clin Infect Dis 46: 7077.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40.

    Billeter SA, Diniz PP, Jett LA, Wournell AL, Kjemtrup AM, Padgett KA, Yoshimizu MH, Metzger ME, Barr MC, 2016. Detection of Rickettsia species in fleas collected from cats in regions endemic and nonendemic for flea-borne rickettsioses in California. Vector Borne Zoonotic Dis 16: 151156.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41.

    Reeves WK, Nelder MP, Korecki JA, 2005. Bartonella and Rickettsia in fleas and lice from mammals in south Carolina, USA. J Vector Ecol 30: 310315.

  • 42.

    Odhiambo AM, Maina AN, Taylor ML, Jiang J, Richards AL, 2014. Development and validation of a quantitative real-time polymerase chain reaction assay specific for the detection of Rickettsia felis and not Rickettsia felis-like organisms. Vector Borne Zoonotic Dis 14: 476481.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43.

    Parola P, Sanogo OY, Lerdthusnee K, Zeaiter Z, Chauvancy G, Gonzalez JP, Miller RS, Telford SR 3rd, Wongsrichanalai C, Raoult D, 2003. Identification of Rickettsia spp. and Bartonella spp. from the Thai-Myanmar border. Ann N Y Acad Sci 990: 173181.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44.

    Oteo JA, Portillo A, Portero F, Zavala-Castro J, Venzal JM, Labruna MB, 2014. ‘Candidatus Rickettsia asemboensis’ and Wolbachia spp. in Ctenocephalides felis and Pulex irritans fleas removed from dogs in Ecuador. Parasit Vectors 7: 455.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 45.

    Fang R, Raoult D, 2003. Antigenic classification of Rickettsia felis by using monoclonal and polyclonal antibodies. Clin Diagn Lab Immunol 10: 221228.

  • 46.

    Hawley JR, Shaw SE, Lappin MR, 2007. Prevalence of Rickettsia felis DNA in the blood of cats and their fleas in the United States. J Feline Med Surg 9: 258262.

  • 47.

    Williams M, Izzard L, Graves SR, Stenos J, Kelly JJ, 2011. First probable Australian cases of human infection with Rickettsia felis (cat-flea typhus). Med J Aust 194: 4143.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 48.

    Lim MY, Brady H, Hambling T, Sexton K, Tompkins D, Slaney D, 2012. Rickettsia felis infections, New Zealand. Emerg Infect Dis 18: 167169.

  • 49.

    Gerhold RW, Jessup DA, 2013. Zoonotic diseases associated with free-roaming cats. Zoonoses Public Health 60: 189195.

  • 50.

    Persichetti MF, Solano-Gallego L, Serrano L, Altet L, Reale S, Masucci M, Pennisi MG, 2016. Detection of vector-borne pathogens in cats and their ectoparasites in southern Italy. Parasit Vectors 9: 247.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 51.

    Ravicini S, Pastor J, Hawley J, Brewer M, Castro-Lopez J, Beall M, Lappin MR, 2016. Prevalence of selected infectious disease agents in stray cats in Catalonia, Spain. JFMS Open Rep 2: 2055116916634109.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 52.

    Levy JK, Crawford PC, 2004. Humane strategies for controlling feral cat populations. J Am Vet Med Assoc 225: 13541360.

  • 53.

    Akucewich LH, Philman K, Clark A, Gillespie J, Kunkle G, Nicklin CF, Greiner EC, 2002. Prevalence of ectoparasites in a population of feral cats from north central Florida during the summer. Vet Parasitol 109: 129139.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 54.

    Green JS, Singh J, Cheung M, Adler FC, Ashouri N, 2011. A cluster of pediatric endemic typhus cases in Orange County, California. Pediatr Infect Dis J 30: 163165.

  • 55.

    Croker C, Foo C, 2015. Multi-agency response to a flea-borne typhus outbreak. Los Angels County Department of Public Health, Acute Communicable Disease Control, 2015 Special Studies Report, 6571. Available at: http://publichealth.lacounty.gov/acd/reports/2015SpecialStudiesReport.pdf. Accessed November 24, 2017.

    • PubMed
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 190 150 16
Full Text Views 1353 15 1
PDF Downloads 184 13 2
 
 
 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save